Coordinated responses to honey bee decline in the USA

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Coordinated responses to honey bee decline in the USA

Jeffery S. Pettis, Keith S. Delaplane

To cite this version:

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Apidologie 41 (2010) 256–263 Available online at: c

INRA/DIB-AGIB/EDP Sciences, 2010 www.apidologie.org DOI:10.1051/apido/2010013

Review article

Coordinated responses to honey bee decline in the USA

*

Je

ﬀery S. P

ettis

1

_{, Keith S. D}

elaplane

2

1_{USDA-ARS Bee Research Laboratory, 476 BARC-E, Beltsville, MD 20705, USA} 2_{Department of Entomology, University of Georgia, Athens, GA 30602, USA}

Received 9 October 2009 – Revised 28 January 2010 – Accepted 2 February 2010

Abstract – In response to successive years of high honey bee mortality, the United States Congress man-dated the US Department of Agriculture (USDA) to increase funding for research and education directed at reducing honey bee decline. The funding follows two administrative streams within USDA – one through the USDA Agricultural Research Service (ARS) and another through the USDA National Institute for Food and Agriculture (NIFA). ARS is funding an Areawide Project operated by the four ARS honey bee labs, and NIFA is funding through a competitive grant process a Coordinated Agricultural Project (CAP) operated by scientists and educators heavily represented by state colleges of agriculture. Each project – Areawide and CAP – is characterized as a consortium of investigators working in a coordinated manner to reduce institutional redundancy and optimize the discovery and delivery of sustainable bee management practices to client beekeepers.

Apis mellifera/ pollinator decline / colony collapse disorder / CCD / research / education / honey bees / Nosema/ integrated pest management / nutrition

1. INTRODUCTION

Honey bee decline in the United States is nothing new. Data collected by the US De-partment of Agriculture (USDA) show a pat-tern of steady decline in the numbers of man-aged hives from a peak of nearly 6 million in the 1940s to 2.3 million by 2008 (Fig.1). The suspected causes for this are many and include trans-global pathogens and parasites (Ellis and Munn,2005) as well as socioeco-nomic trends that serve to push beekeepers out of practice, as seems to be the case throughout virtually all of Europe (Potts et al.,2010). This downward spiral in the United States went from bad to worse in the opening decade of this century. In the winter of 2004–2005, bee-keepers began reporting unusual colony losses in California where colonies were collapsing in advance of almond pollination in Febru-Corresponding author: J.S. Pettis,

jeﬀ.pettis@ars.usda.gov

* Manuscript editor: Marla Spivak

ary and March of 2005. A survey of strong and weak colonies in seven commercial oper-ations representing six states failed to point to any one cause when evaluations by the USDA Beltsville Laboratory were limited to para-sitic mites, Nosema and viruses (Anonymous,

2005). In the fall of 2005, following contin-ued reports of colony and queen problems, a meeting of approximately 40 industry leaders and researchers was held in Lincoln, Nebraska to discuss colony declines. No definitive con-clusions were reached, but all in attendance agreed that colony losses and queen problems were greater in scope than in previous years; this seemed to hold true even for beekeep-ing operations that had changed little over the past 20 years, even with the acknowledged im-pact of Varroa. The group also considered the role of pesticides, both in-hive (Pettis et al.,

2004) and agricultural (Nguyen et al.,2009). Following this meeting, the USDA initiated a nutrition and bee stock study in Bakers-field, California and found that supplemental

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Coordinated responses in the USA 257

Figure 1. The number of managed honey bee colonies (in millions) in the United States from 1945 to 2008 as reported by the USDA National Agricultural Statistics Service. The current level of approximately 2.5 million colonies is very low given that the US needs 1.5 million colonies in California each year to pollinate almonds. Three years of on average 30% colony losses in the US (2006–2008) threaten our ability to provide such pollination services to agriculture. No data on colony numbers were recorded for 1982– 1985.

feeding stabilized colony strength but did lit-tle to increase colony size for almond polli-nation (DeGrandi-Hoﬀman et al.,2008). This reduction in managed colonies, coupled with increased colony mortality, has resulted in in-creased pollination fees for almonds and other crops; for example, in almonds the fee per colony has risen from $75 to $150 and in blueberries a similar doubling of pollination fees has occurred. The almond industry alone needs 1.5 million colonies annually for pol-lination, more than half the nation’s colony reserves. Even though beekeepers can par-tially recover winter losses with spring-time splits (managed colony division), this prac-tice cannot compensate for successive win-ter losses hovering near 30% (vanEngelsdorp et al.,2008,2010). In this sense the situation in the US is more grave than that reported by Aizen and Harder (2009) for the global scale. Those authors showed that the global area of pollinator-dependent crops is increasing faster than the growth in global reserves of bee hives. In the US the increase in pollinator-dependent

crops is accompanied by a decrease in the na-tional reserve of bee hives. More than anything else, this fact constitutes the nexus of the per-ceived pollinator deficit in US agriculture.

Among the dead colonies piling up during these years was a group expressing a delim-iting set of symptoms – a condition which has come to be called Colony Collapse Disorder or CCD. The symptoms assigned to CCD include (1) the dwindling or near complete loss of adult bees with few or no dead bees around the hive, (2) low ratio of adult bees to remaining brood, (3) a disproportionately young work-force, (4) reluctance of dwindling colonies to consume food provided by the beekeeper, and (5) reluctance of neighboring bees to rob the colony once it is dead (Ellis et al., 2010; vanEngelsdorp et al.,2010). Colonies catego-rized with CCD were subsequently shown pos-itive for multiple pathogens, including virus and Nosema spp., and there is evidence that the causative agents are communicable (Cox-Foster et al., 2007; vanEngelsdorp et al.,

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258 J.S. Pettis, K.S. Delaplane

by some American scientists who view it as too symptom based which takes away from objective attempts to assign etiology and cau-sation to bee disorders. At the very least it is important to desynonymize CCD from bee de-cline in general. Bees die from many things, and CCD is just one of them (Neumann and Carreck,2010; Genersch et al.,2010, this is-sue). From a scientific perspective, CCD is best thought of as a syndrome – a set of symp-toms inviting scrutiny by experimenters armed with Koch’s Postulates and intent on parcel-ing out the constituent or interactparcel-ing agents. In beekeeper surveys, the fraction of U.S. colony winter deaths attributed to CCD has ranged from 36–60% (vanEngelsdorp et al.,2010).

In October 2006, the National Research Council released its seminal report, Status of Pollinators in North America (NRC, 2007), awakening a general awareness of the decline of honey bees and other pollinators. The NRC report was followed by three papers document-ing successive colony mortality in the United States for the winters of 2006–2009 at 32%, 36% and 29% (vanEngelsdorp et al., 2007,

2008,2010) and yet more papers reinforcing that colony numbers are necessarily important to global agriculture (Klein et al.,2007) and at the same time failing to keep pace with a growing demand for pollinator-dependent crops (Aizen and Harder,2009). The reaction by beekeepers and the public has been imme-diate and sustained. Meetings and Congres-sional hearings were held in 2007 and 2008 and a CCD Action Plan was drafted to serve as a guide to a coordinated national research and education response aimed at reversing honey bee decline.

The agency charged to administer these Congressional mandates is the cabinet-level US Department of Agriculture (USDA), and within USDA the two divisions most directly involved with bee research are the Agricul-tural Research Service (ARS) and the National Institute for Food and Agriculture (NIFA), formerly known as the Cooperative State Research, Education, and Extension Service (CSREES). Each of these divisions represents a funding stream for one of the two coordi-nated projects described in this paper.

ARS is the administrative home of the five federal bee labs, including the Bee Research Laboratory in Beltsville, Maryland, special-izing in honey bee diseases and pests; the Honey Bee Breeding, Genetics, and Physiol-ogy Laboratory in Baton Rouge, Louisiana, dedicated to improving honey bee stock and honey bee management; the Honey Bee Re-search Unit at Weslaco, Texas, emphasizing studies on Africanized honey bees and man-agement of honey bee parasites and stresses; the Carl Hayden Bee Research Center in Tuc-son, Arizona, concentrating on bee nutrition, pollination, and management of Africanized bees and Varroa mites; and the Bee Biology and Systematics Laboratory in Logan, Utah, the unit dedicated to the biology, systematics, and management, of non-Apis bees.

NIFA is the main conduit for competitive federal grant dollars flowing from Washington to non-federal research and education institu-tions across the US, most of which are colleges of agriculture in state universities. The begin-nings of this system can be traced to the Mor-rill Act, signed into law by President Abraham Lincoln in 1862, creating the so-called Land Grant system which incentivized states to es-tablish “colleges for the benefit of agricul-ture and mechanic arts” (NIFA,2009a). A sec-ond Morrill Act of 1890 provided incentives for states to establish colleges of “agriculture and mechanic arts” for historically disadvan-taged populations (NIFA,2009b). Combined, the Morrill Acts have been recognized as syn-ergists for the increase of equal-opportunity education in the United States, drivers for the extension of research-based knowledge into America’s rural communities, and partial ex-planations for America’s rise as a technologi-cal society in the 20th century. Today, a signif-icant portion of the bee research in the United States, and virtually all of the institutional bee-keeping education in the United States, come from universities in the Land Grant system.

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and puts a premium on deliverable results. Not one, but two coordinated schemes have emerged from the Congressional mandate – the Areawide Project administered by ARS and the Coordinated Agricultural Project (CAP) administered by NIFA. Each of us is the national director for his respective program – JSP for Areawide and KSD for CAP – and here we give an overview of our programs, their ob-jectives, points of shared collaborations, and expected outcomes. It is not our intent in this paper to review the published experimental material related to colony losses nor the his-tory of losses in the US the but rather to con-centrate on more recent colony losses and the coordinated research eﬀort that has developed in the US.

2. USDA-ARS AREAWIDE PROJECT TO IMPROVE HONEY BEE HEALTH

This program will conduct a comprehensive set of demonstration trials across the country bringing together recent ARS research find-ings on mite-resistant bee stocks, improved di-ets, mite and disease control alternatives, and general colony management techniques. Each of the four ARS honey bee labs will be respon-sible for a distinct area of research, but in the case of parasite and pest control and migra-tory stress reduction some overlap is needed to take advantage of the expertise present in each laboratory. Economic analyses of the var-ious management techniques will be carried out and the findings communicated to stake-holders over the life of the program. The pro-gram will involve the interplay between four broad components that impact colony health: (1) bee stock, (2) nutrition, (3) pests and dis-ease control and (4) colony management tech-niques.

The overarching goal of the Areawide pro-gram is to increase colony survival and avail-ability for pollination and thus increase the profitability of beekeeping in the US. To this end, it has enumerated the following objec-tives:

1. To increase colony strength for pollination of almonds and subsequent crops.

2. To demonstrate that resistant bee stocks re-duce operating costs and increase survivor-ship.

3. To demonstrate improved parasitic mite control with proper timing of application. 4. To improve the content and delivery

meth-ods for carbohydrate and protein diets. 5. To improve the integrated use of

con-trols for pests and diseases including non-chemical beekeeping methodology. The Baton Rouge lab will focus on bee stock improvement and evaluations and improving early spring buildup using genetic selection and colony size. Special attention will be fo-cused on two ARS bee stock improvements – Russian bees and the Varroa Sensitive Hy-giene (VSH) trait (Baton Rouge) (Rinderer et al., 2010). The Beltsville lab will fo-cus on improving queen longevity, improv-ing Nosema controls, investigatimprov-ing the antibi-otic Tylosin, improving non-chemical Varroa limiters such as plastic drone comb and screen bottom boards, and identifying and mitigating stressors associated with migratory beekeep-ing. The Tucson lab will concentrate on nutri-ent supplemnutri-ents including carbohydrates and the protein supplement Mega Beeas well as the miticidal properties of 2-heptanone. The Weslaco lab will be working on improved management techniques for Varroa including the miticide Hivastan, along with new con-trols for Nosema, stock improvements with Africanized bees, and mitigating stress asso-ciated with migratory beekeeping.

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strength parameters. Collectively, these twin projects will give an unprecedented descrip-tion of the state of American honey bees with insight into the comparative impacts of station-ary versus migratory practices.

In all these eﬀorts we will involve univer-sity partners in economic analysis and exten-sion. Technology and knowledge transfer from the Areawide Program will be a group ef-fort with assistance from the American Asso-ciation of Professional Apiculturists (AAPA) and university personnel, most particularly the CAP program who will conduct beekeeping workshops and field days as part of their man-date for knowledge delivery. The most con-spicuous partnership, already launched, is the Bee Health Community of Practice website

http://www.extension.org/bee_health, a shared collaboration between the Areawide Program and all entities named above. One of the most important products on this site will be a Best Management Practices literature, regularly up-dated, and representing the latest science-based recommendations for bee management. There continue to be emerging issues in the management of honey bees that may require additional research and extension eﬀorts over the life of this project. One example is the recognition of a second species of the internal parasitic microsporidian Nosema spp. Another is the CCD phenomenon for which researchers have implicated candidate pathogens (Cox-Foster et al.,2007; vanEngelsdorp et al.,2009) and mechanistic pathways (Johnson et al.,

2009). Issues such as these, and new ones, can be expected over the life of the five-year Areawide project and our management scheme must remain flexible to accommodate emerg-ing priorities.

3. NIFA COORDINATED AGRICULTURAL PROJECT

The CAP concept, an innovation of the National Institute for Food and Agriculture (NIFA), is applied broadly to agricultural problems of a national scale. NIFA solicits and awards no more than one CAP project per year. CAP projects are state, multi-institutional, multi-year, national in scope, and

integrate research with information delivery to client publics. The idea is to eliminate re-dundancy and create a seamless transition be-tween new research and the stakeholders who can use it. Examples of other CAP projects in-clude Avian Influenza, Porcine Reproductive and Respiratory Syndrome, and Johne’s Dis-ease in cattle. 2008 was the year for Managed Pollinators, and funding was made available at the level of $4.1 million for 4 years. A con-sortium of over 20 research and extension spe-cialists emerged from a competitive proposal process, representing 18 institutions, includ-ing fifteen 1862 Land Grant institutions, one 1890 institution, and two ARS bee labs.

Our approach has been to assume that bee decline is a product of numerous interact-ing factors, synthetic and organic. Late re-search seems to bear this out. Colonies ex-pressing symptoms associated with CCD – rapid loss of adult bees and low ratios of adult bees to brood – have been shown to ex-press high rates of mixed infections, including viruses and Nosema species (vanEngelsdorp et al., 2009). If viruses are shown to dis-rupt fundamental processes such as RNA tran-scription (Johnson et al., 2009) and immune response, this could explain the kind of wide-scale generic bee morbidities described in re-cent years. At the field level, beekeepers report many suspected causes of winter mortality, the latest data coming from a survey of 2008– 2009 winter losses in which beekeepers ranked the following as the top nine contributing fac-tors: starvation, queens, weather, mites, weak in fall, Nosema, management, CCD, and pesti-cides (vanEngelsdorp et al.,2010). And finally, the ubiquity and variety of pesticide residues inside bee hives (Frazier et al., 2008) further strengthen the view that a broad exploratory approach is justified at this early stage of our researches.

Working from this starting point, our con-sortium has organized itself around four broad objectives:

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2. Incorporate traits that help honey bees re-sist pathogens and parasitic mites and in-crease genetic diversity of commercially available stocks.

3. Improve conservation and management of non-Apis pollinators by identifying new or emerging pathogens and parasites, abiotic stresses, habitat degradation, and practices that optimize their pollinating eﬃcacy. 4. Deliver research knowledge to client

groups by developing a technology trans-fer program for queen breeders and a liter-ature on Best Management and Conserva-tion.

Details of the working objectives under each of these goals, including specific collabora-tors, rationale, and expected outcomes, are viewable at our dedicated websitehttp://www.

beeccdcap.uga.edu/. But for our purposes here we give a general overview below.

For goal 1 we are engaged in experi-ments designed to characterize bee morbid-ity associated with Nosema apis and N.

cer-anae; to characterize epidemiology of

Is-raeli acute paralysis virus and deformed wing virus; to monitor with a standardized sampling scheme the pathogen and pesticide loads in each of seven stationary apiaries in the states of California, Washington, Texas, Minnesota, Florida, Pennsylvania, and Maine; to design diagnostic tools for high-throughput detection of diseases; and to improve basic toxicology on in-hive acaricides and some of the newer generation agricultural pesticides.

The seven-state stationary apiary monitor-ing scheme described above is one of the points of collaboration between the two coor-dinated projects described in this paper. Data from the stationary apiaries will be joined with data from colonies managed in a migratory fashion typical for much of the commercial beekeepers in the US and monitored by ARS Areawide. It is hoped that this design will not only give a representative picture of the state of honey bees in the US, but also elucidate the comparative eﬀects of management on honey bee health.

Goal two is designed under the assumption that bee breeding and the conservation of ge-netic diversity in Apis mellifera in the United

States are good investments in bee health man-agement that is sustainable and independent of alien chemicals in the bee nest environment. To that end, we have designed research pro-grams to identify genes that confer honey bee resistance to Varroa destructor and other bi-otic stressors. A second working objective is aimed at identifying geographically discrete pockets of honey bee genetic diversity.

The third goal represents our investment in non-Apis pollinators. Here we have designed experiments that mirror the pathology and tox-icology work in goal one with A. mellifera. The mirroring is especially conspicuous in the case of the stationary apiary monitoring scheme in which the collaborators will be do-ing systematic sampldo-ing on-site for non-Apis bees and subjecting these samples to disease and pesticide analysis to check for cross-over disorders between bee taxa.

The fourth and final goal represents our in-vestment in one of the pillars of the CAP con-cept – client delivery. Here we have taken steps to inaugurate face-to-face training sessions for commercial queen breeders in California – the industry sector representing the largest source of queens sold annually in the US – in the methods of genetic selection for dis-ease and mite resistance. Preliminary eﬀorts on the ground have been met with enthusias-tic support by the client group. In another ex-ample of collaboration between ARS Areaw-ide and CAP, the two groups have partnered to create a “Bee Health” web site at eXten-sion.org – viewable at http://www.extension.

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the topic. In its mature state the Bee Health website is envisioned to become the most com-plete and authoritative compendium of liter-ature on bee health management that science can oﬀer.

4. EXPECTED OUTCOMES

It is to be hoped that the unprecedented de-gree of coordination between the two projects described here will optimize the speed with which practical improvements to bee health management can be discovered and delivered to beekeepers. We believe that the breadth of each project is appropriately broad, reflecting the uncertain state of our knowledge on the many factors interacting to impair honey bee health. At the same time, the objectives of each project seem reasonably narrow – likely, we believe, to hit close to the mark in our search for the morbidity agents most responsible for honey bee decline. Insofar as we can narrow the list of candidate agents, refine research priorities, and eﬀectively deliver to beekeep-ers the best science-based management recom-mendations, these projects will prove a solid investment for the sustainability of America’s beekeeping industry.

Réponses coordonnées au déclin des abeilles aux États-Unis.

Apis mellifera/ déclin des pollinisateurs / CCD / syndrome d’eﬀondrement des colonies / re-cherche/ éducation / abeilles / Nosema / lutte inté-grée/ nutrition

Zusammenfassung – Koordinierte Antworten auf die Abnahme von Honigbienen in den USA. Daten über imkerlich gehaltene Bienenvöl-ker vom US amerikanischen Landwirtschaftsmini-sterium (US Department of Agriculture, USDA) zeigen eine kontinuierliche Abnahme der Bienen-völker vom Spitzenwert von 6 Mio. in den 1940er Jahren auf 2,3 Mio. im Jahr 2008 (Abb.1). Die ver-mutlichen Ursachen für diesen Rückgang sind viel-fältig. Sie beinhalten trans-globale Pathogene und Parasiten und sozio-ökonomische Trends, die Imker aus ihrer Praxis drängen, was in ganz Europa der Fall ist. Zusätzlich sind unter den toten Völkern aus der jüngsten Vergangenheit eine Gruppe mit abge-grenzten Symptomen, die als „colony collapse dis-order (CCD)“ bezeichnet wurden. Die

Hauptsymp-tome des CCD sind Schwund oder nahezu vollstän-diger Verlust adulter Bienen und ein geringer An-teil von Adultbienen zu Brut. Die generelle Abnah-me der Völkerzahlen, zusamAbnah-men mit einer erhöhten Mortalität aufgrund von CCD und anderen Fakto-ren, führte zu einer Verteuerung der Bestäubungs-prämie für Mandeln und anderen Nutzpflanzen. In den Vereinigten Staaten wird der Anstieg der be-stäubungsabhängigen Nutzpflanzen von einer Ab-nahme des nationalen Bienenvölkervorrats beglei-tet, eine ernste Situation für die landwirtschaftliche Bestäubung.

Als Reaktion auf die hohe Honigbienensterblich-keit der vergangenen Jahre beauftragte der US Con-gress das US Landwirtschaftsministerium damit, solche Forschungs- und Bildungsförderung zu stei-gern, die auf eine Reduktion der Honigbienenab-nahme gerichtet sind. Der Landwirtschaftliche For-schungsdienst der USA (USDA-ARS) fördert ein von vier ARS Laboratorien durchgeführtes, soge-nanntes Areawide Projekt. Das USDA National In-stitute for Food and Agriculture fördert ein ko-ordiniertes Landwirtschaftsprojekt (CAP), welches vornehmlich von Wissenschaftlern und Pädagogen aus staatlichen landwirtschaftlichen Colleges be-trieben wird. Beide Projekte, Areawide und CAP, sind durch ein Konsortium von Forschern charak-terisiert, die koordiniert zusammenarbeiten, um in-stitutionelle Redundanz zu reduzieren und die Ent-deckung und Verbreitung einer nachhaltigen Imke-rei zu optimieren.

Das übergeordnete Ziel des USDA-ARS Areawide Programms ist es, das Überleben der Völker und die Verfügbarkeit für Bestäubung zu erhöhen. Der

CAP-Ansatz geht davon aus, dass die

Bienenabnah-me ein Produkt zahlreicher interagierender Fakto-ren ist: synthetische und organische. Daraus sollen Versuche um die spezifischen Faktoren der Völker-verluste entwickelt werden. Der Technologie- und Wissenstransfer vom Areawide Programm und CAP Programmen wird ein Gruppenaufwand mit Unter-stützung des Verbandes der amerikanischen Berufs-simker (American Association of Professional Api-culturists: AAPA ) sein. Die auﬀälligste bereits lan-cierte Partnerschaft ist die Webseite der Gemein-schaft zur Bienengesundheit und Praxis (Bee

He-alth Community of Practice,http://www.extension. org/bee_health). Es ist eine Kollaboration zwischen dem Areawide Programm und allen oben genannten Programmen. Beide Projekte, Areawide und CAP werden daran arbeiten, die Gesundheit der Bienen-völker zu verbessern und wissenschaftlich fundier-te Lösungen anzubiefundier-ten um die Bienenhaltung und das Überleben der Bienen zu verbessern.

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